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Genomic Changes Associated with Adaptation to Arid Environments in Cactophilic Drosophila Species

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Genomic Changes Associated with Adaptation to Arid Environments in Cactophilic Drosophila Species Genomic changes associated with adaptation to arid environments in cactophilic Drosophila species Rane, Rahul V.; Pearce, Stephen L.; Li, Fang; Coppin, Chris; Schiffer, Michele; Shirriffs, Jennifer; Sgro, Carla M.; Griffin, Philippa C.; Zhang, Goujie; Lee, Siu F.; Hoffmann, Ary A.; Oakeshott, John G Published in: BMC Genomics DOI: 10.1186/s12864-018-5413-3 Publication date: 2019 Document version Publisher's PDF, also known as Version of record Document license: CC BY Citation for published version (APA): Rane, R. V., Pearce, S. L., Li, F., Coppin, C., Schiffer, M., Shirriffs, J., Sgro, C. M., Griffin, P. C., Zhang, G., Lee, S. F., Hoffmann, A. A., & Oakeshott, J. G. (2019). Genomic changes associated with adaptation to arid environments in cactophilic Drosophila species. BMC Genomics, 20, 1-22. [52]. https://doi.org/10.1186/s12864- 018-5413-3 Download date: 01. Oct. 2021 Rane et al. BMC Genomics (2019) 20:52 https://doi.org/10.1186/s12864-018-5413-3 RESEARCH ARTICLE Open Access Genomic changes associated with adaptation to arid environments in cactophilic Drosophila species Rahul V. Rane1,2* , Stephen L. Pearce1, Fang Li3, Chris Coppin1, Michele Schiffer2, Jennifer Shirriffs2, Carla M. Sgrò4, Philippa C. Griffin2, Goujie Zhang3,5, Siu F. Lee1,2, Ary A. Hoffmann2 and John G. Oakeshott1 Abstract Background: Insights into the genetic capacities of species to adapt to future climate change can be gained by using comparative genomic and transcriptomic data to reconstruct the genetic changes associated with such adaptations in the past. Here we investigate the genetic changes associated with adaptation to arid environments, specifically climatic extremes and new cactus hosts, through such an analysis of five repleta group Drosophila species. Results: We find disproportionately high rates of gene gains in internal branches in the species’ phylogeny where cactus use and subsequently cactus specialisation and high heat and desiccation tolerance evolved. The terminal branch leading to the most heat and desiccation resistant species, Drosophila aldrichi, also shows disproportionately high rates of both gene gains and positive selection. Several Gene Ontology terms related to metabolism were enriched in gene gain events in lineages where cactus use was evolving, while some regulatory and developmental genes were strongly selected in the Drosophila aldrichi branch. Transcriptomic analysis of flies subjected to sublethal heat shocks showed many more downregulation responses to the stress in a heat sensitive versus heat resistant species, confirming the existence of widespread regulatory as well as structural changes in the species’ differing adaptations. Gene Ontology terms related to metabolism were enriched in the differentially expressed genes in the resistant species while terms related to stress response were over-represented in the sensitive one. Conclusion: Adaptations to new cactus hosts and hot desiccating environments were associated with periods of accelerated evolutionary change in diverse biochemistries. The hundreds of genes involved suggest adaptations of this sort would be difficult to achieve in the timeframes projected for anthropogenic climate change. Keywords: Comparative genomics, Transcriptomics, Cactophilic Drosophila, Heat stress, Host adaptation Background because many of its species have diverged in their re- One approach to assessing the ability of species to adapt sponses to climatic extremes [2–4]. genetically to future climate change is to reconstruct the One particularly promising species group to study in way such adaptation has occurred in the past. The best this respect is the repleta group (subgenus Drosophila), way to do this is to compare the genomes of closely re- which originated about 15 million years ago in the lated species that have diverged for the relevant pheno- Americas [5]. Many species in this group, such as the types, but where genetic changes due to drift or other mulleri subgroup species Drosophila mojavensis, D. buz- adaptations irrelevant to those phenotypes are minimal zatii and D. aldrichi, are desert-adapted and display ex- [1]. Drosophila is an ideal genus for such an analysis tremely high heat, cold and desiccation tolerance [2, 3] but other species, such as the hydei and repleta sub- group species D. hydei and D. repleta, are largely found * Correspondence: [email protected] outside the desert and are much less tolerant of these 1 CSIRO, Clunies Ross St, GPO Box 1700, Acton, ACT 2601, Australia stresses [2, 3, 6]. Notably also, while all the repleta group 2Bio21 Institute, School of BioSciences, University of Melbourne, 30 Flemington Road, Parkville 3010, Australia species are saprophagous (feed on rotting tissue) they Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Rane et al. BMC Genomics (2019) 20:52 Page 2 of 22 vary widely in their host preferences; the desert species model prediction for that species. We present new ge- are dietary specialists that feed and breed on necrotic nomes for the other three species, acknowledging that an- cactus tissue, whereas D. hydei and D. repleta are dietary other version of the D. hydei genome has also recently generalists which can utilise a wide range of rotting been published ([23] and see below). Comparative analyses fruits and vegetables, as well as animal faeces and, in the among these four genomes plus D. mojavensis,andbe- case of D. hydei, cacti as well [7–10]. tween the five repleta species and previously published ge- Some comparative genomic studies have been con- nomes from other Drosophila groups, are then used to ducted on two repleta group species, the cactophilic D. suggest genetic factors contributing to high temperature mojavensis and D. buzzatii. Both are relatively tolerant tolerance and cactus vs generalist dietary adaptations. to climate stresses [5, 11, 12] but the former is much These analyses are founded on a robust genome-wide more restricted geographically and in the range of cacti phylogeny for a total of 24 Drosophila species for which it will use [13]. Comparisons between these two species good quality genomes were available at the time [24]. and two other drosophilids outside the repleta species Orthologue and duplication predictions and branch site group (D. virilis and D. grimshawi) showed expansions modelling are then used to identify lineage-specific gene of gene families involved in proteolysis, sensory percep- expansions and bursts of positive selection in the repleta tion and gene regulation in the cactophilic species [5]. species group. We also compare transcriptomes across a The same study also found the cactophilic species were time course of heat shock response for the heat sensitive undergoing rapid positive selection in genes involved in D. hydei and heat tolerant D. buzzatii, and test whether gene regulation and the catabolism of some of the het- gene sets showing divergent transcriptomic responses to erocyclic toxins found in the cacti [5]. Transcriptomic heat between these species are related to those showing comparisons of populations living on different hosts genomic divergence. within both D. mojavensis and another repleta species group cactophile, D. mettleri, have also highlighted tran- Results scriptional changes in key metabolic and sensory path- Genome assemblies and annotations ways which might contribute to desiccation and/or host Among the three newly sequenced species, the highly in- adaptation [12, 14–16]. There is thus evidence for both bred D. hydei and D. repleta lines had better assembly regulatory and structural changes, in the form of gene statistics than the D. aldrichi line, which was less inbred gains as well as positive selection, associated with the ac- than the other two (see Materials and Methods and quisition of cactophilism in the repleta group. However Additional file 1: Text S2). This is apparent from the lar- interpretation of the associations is limited by the few ger scaffolds and smaller scaffold L50 s for D. hydei and species studied and in some cases the substantial phylo- D. repleta compared to D. aldrichi (Additional file 2: genetic distance involved in the comparison. Table S1). The D. hydei assembly also had superior as- Several genome-wide association (GWAS) studies sembly (and annotation) statistics to the other recently have also found quantitative trait loci (QTLs) contribut- published version of this genome [23]; compared to the ing to polymorphic variation in thermal and desiccation other version, our assembly had an N50 three times lar- stress traits within D. melanogaster [17–20]. Associa- ger and covered 90% of the genome in less than half the tions have been recorded with hundreds of different number of scaffolds (Additional file 2: Tables S1, S2). genes, including a number of heat shock proteins, but The generalist feeders D. hydei and D. repleta yielded their relevance to the cactophilic repleta species is assembled genome sizes of ~ 165 Mb, which is very close questionable because of the ecological differences and to previous estimates generated using DAPI staining phylogenetic distance involved, and the fact that most (177+/− 22 and 167+/− 13 Mb respectively; [25]). No of the D. melanogaster studies are based on microarray DAPI estimate has been published for the cactophilic D. rather than sequencing data. aldrichi but our assembled genome size (191 Mb) for To follow up the work on the cactophilic species above, this species was larger than the two generalists but simi- the current study investigates gene gains and positive se- lar to that previously published for the cactophilic D.
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